The mitochondrial fluorescent dye rhodamine 123 is a high-affinity substrate for organic cation transporters (OCTs) 1 and 2

Fundamental and Clinical Pharmacology

Volumn 28, Issue 1, 2014, Pages 65-77

  Jouan, Elodie ^a   Le Vee, Marc ^a   Denizot, Claire ^b   Da Violante, Georges ^b   Fardel, Olivier ^a,c  

^a UNIVERSITÉ DE RENNES 1   (France)

^b INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

^c RENNES UNIVERSITY HOSPITAL   (France)

Author keywords

Drug transport; Organic cation transporter 1; Organic cation transporter 2; Rhodamine 123

Indexed keywords

AMITRIPTYLINE; DRUG CARRIER; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; PRAZOSIN; QUININE; RHODAMINE 123; TETRYLAMMONIUM; VERAPAMIL;

ACTIVE TRANSPORT; ARTICLE; CELL MEMBRANE TRANSPORT; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG TRANSPORT; DRUG UPTAKE; EMBRYO; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; PHARMACOLOGICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

DRUG TRANSPORT; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; RHODAMINE 123;

BIOLOGICAL TRANSPORT; CELL LINE; FLUORESCENT DYES; HEK293 CELLS; HUMANS; MITOCHONDRIA; ORGANIC CATION TRANSPORT PROTEINS; ORGANIC CATION TRANSPORTER 1; RHODAMINE 123; TETRAETHYLAMMONIUM;

EID: 84892514301     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/j.1472-8206.2012.01071.x     Document Type: Article

References (57)

1. Johnson L.V., Walsh M.L., Chen L.B. Localization of mitochondria in living cells with rhodamine 123. Proc. Natl. Acad. Sci. USA (1980) 77 990-994.
2. Johnson L.V., Walsh M.L., Bockus B.J., Chen L.B. Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol. (1981) 88 526-535.
3. Chaudhary P.M., Roninson I.B. Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell (1991) 66 85-94.
4. Fardel O., Lecureur V., Guillouzo A. The P-glycoprotein multidrug transporter. Gen. Pharmacol. (1996) 27 1283-1291.
5. Efferth T., Lohrke H., Volm M. Reciprocal correlation between expression of P-glycoprotein and accumulation of rhodamine 123 in human tumors. Anticancer Res. (1989) 9 1633-1637.
6. Ludescher C., Thaler J., Drach D. et al. Detection of activity of P-glycoprotein in human tumour samples using rhodamine 123. Br. J. Haematol. (1992) 82 161-168.
7. Drenou B., Fardel O., Amiot L., Fauchet R. Detection of P glycoprotein activity on normal and leukemic CD34 + cells. Leuk. Res. (1993) 17 1031-1035.
8. Coon J.S., Wang Y.Z., Bines S.D., Markham P.N., Chong A.S., Gebel H.M. Multidrug resistance activity in human lymphocytes. Hum. Immunol. (1991) 32 134-140.
9. Doyle L.A., Ross D.D. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene (2003) 22 7340-7358.
10. Honjo Y., Hrycyna C.A., Yan Q.W. et al. Acquired mutations in the MXR/BCRP/ABCP gene alter substrate specificity in MXR/BCRP/ABCP-overexpressing cells. Cancer Res. (2001) 61 6635-6639.
11. Munic V., Hlevnjak M., Erakovic Haber V. Characterization of rhodamine-123, calcein and 5(6)-carboxy-2', 7'-dichlorofluorescein (CDCF) export via MRP2 (ABCC2) in MES-SA and A549 cells. Eur. J. Pharm. Sci. (2011) 43 359-369.
12. Kim M., Cooper D.D., Hayes S.F., Spangrude G.J. Rhodamine-123 staining in hematopoietic stem cells of young mice indicates mitochondrial activation rather than dye efflux. Blood (1998) 91 4106-4117.
13. Nies A.T., Koepsell H., Damme K., Schwab M. Organic cation transporters (OCTs, MATEs), in vitro and in vivo evidence for the importance in drug therapy. Handb. Exp. Pharmacol. (2011) 201 105-167.
14. Hagenbuch B. Drug uptake systems in liver and kidney: a historic perspective. Clin. Pharmacol. Ther. (2010) 87 39-47.
15. Jonker J.W., Schinkel A.H. Pharmacological and physiological functions of the polyspecific organic cation transporters: OCT1, 2, and 3 (SLC22A1-3). J. Pharmacol. Exp. Ther. (2004) 308 2-9.
16. Koepsell H., Lips K., Volk C. Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm. Res. (2007) 24 1227-1251.
17. Jigorel E., Le Vee M., Boursier-Neyret C., Bertrand M., Fardel O. Functional expression of sinusoidal drug transporters in primary human and rat hepatocytes. Drug Metab. Dispos. (2005) 33 1418-1422.
18. Heemskerk S., Wouterse A.C., Russel F.G., Masereeuw R. Nitric oxide down-regulates the expression of organic cation transporters (OCT) 1 and 2 in rat kidney during endotoxemia. Eur. J. Pharmacol. (2008) 584 390-397.
19. Hirsch-Ernst K.I., Ziemann C., Rustenbeck I., Kahl G.F. Inhibitors of mdr1-dependent transport activity delay accumulation of the mdr1 substrate rhodamine 123 in primary rat hepatocyte cultures. Toxicology (2001) 167 47-57.
20. Annaert P.P., Brouwer K.L. Assessment of drug interactions in hepatobiliary transport using rhodamine 123 in sandwich-cultured rat hepatocytes. Drug Metab. Dispos. (2005) 33 388-394.
21. Le Vee M., Jigorel E., Glaise D., Gripon P., Guguen-Guillouzo C., Fardel O. Functional expression of sinusoidal and canalicular hepatic drug transporters in the differentiated human hepatoma HepaRG cell line. Eur. J. Pharm. Sci. (2006) 28 109-117.
22. Jigorel E., Le Vee M., Boursier-Neyret C., Parmentier Y., Fardel O. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab. Dispos. (2006) 34 1756-1763.
23. Le Vee M., Lecureur V., Stieger B., Fardel O. Regulation of drug transporter expression in human hepatocytes exposed to the proinflammatory cytokines tumor necrosis factor-alpha or interleukin-6. Drug Metab. Dispos. (2009) 37 685-693.
24. Zhang L., Gorset W., Dresser M.J., Giacomini K.M. The interaction of n-tetraalkylammonium compounds with a human organic cation transporter, hOCT1. J. Pharmacol. Exp. Ther. (1999) 288 1192-1198.
25. Ahlin G., Karlsson J., Pedersen J.M. et al. Structural requirements for drug inhibition of the liver specific human organic cation transport protein 1. J. Med. Chem. (2008) 51 5932-5942.
26. Zolk O., Solbach T.F., Konig J., Fromm M.F. Structural determinants of inhibitor interaction with the human organic cation transporter OCT2 (SLC22A2). Naunyn Schmiedebergs Arch. Pharmacol. (2009) 379 337-348.
27. Lee W.K., Reichold M., Edemir B. et al. Organic cation transporters OCT1, 2, and 3 mediate high-affinity transport of the mutagenic vital dye ethidium in the kidney proximal tubule. Am. J. Physiol. Renal Physiol. (2009) 296 F1504-F1513.
28. Kimura H., Takeda M., Narikawa S., Enomoto A., Ichida K., Endou H. Human organic anion transporters and human organic cation transporters mediate renal transport of prostaglandins. J. Pharmacol. Exp. Ther. (2002) 301 293-298.
29. Mehrens T., Lelleck S., Cetinkaya I. et al. The affinity of the organic cation transporter rOCT1 is increased by protein kinase C-dependent phosphorylation. J. Am. Soc. Nephrol. (2000) 11 1216-1224.
30. Kido Y., Matsson P., Giacomini K.M. Profiling of a prescription drug library for potential renal drug-drug interactions mediated by the organic cation transporter 2. J. Med. Chem. (2011) 54 4548-4558.
31. Cheng Y., Prusoff W.H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. (1973) 22 3099-3108.
32. Zhang L., Schaner M.E., Giacomini K.M. Functional characterization of an organic cation transporter (hOCT1) in a transiently transfected human cell line (HeLa). J. Pharmacol. Exp. Ther. (1998) 286 354-361.
33. Gorbunov D., Gorboulev V., Shatskaya N. et al. High-affinity cation binding to organic cation transporter 1 induces movement of helix 11 and blocks transport after mutations in a modeled interaction domain between two helices. Mol. Pharmacol. (2008) 73 50-61.
34. Volk C., Gorboulev V., Kotzsch A., Muller T.D., Koepsell H. Five amino acids in the innermost cavity of the substrate binding cleft of organic cation transporter 1 interact with extracellular and intracellular corticosterone. Mol. Pharmacol. (2009) 76 275-289.
35. Minuesa G., Volk C., Molina-Arcas M. et al. Transport of lamivudine [(-)-beta-L-2', 3'-dideoxy-3'-thiacytidine] and high-affinity interaction of nucleoside reverse transcriptase inhibitors with human organic cation transporters 1, 2, and 3. J. Pharmacol. Exp. Ther. (2009) 329 252-261.
36. Nadakavukaren K.K., Nadakavukaren J.J., Chen L.B. Increased rhodamine 123 uptake by carcinoma cells. Cancer Res. (1985) 45 6093-6099.
37. Hartig S., Fries S., Balcarcel R.R. Reduced mitochondrial membrane potential and metabolism correspond to acute chloroform toxicity of in vitro hepatocytes. J. Appl. Toxicol. (2005) 25 310-317.
38. van der Sandt I.C., Blom-Roosemalen M.C., de Boer A.G., Breimer D.D. Specificity of doxorubicin versus rhodamine-123 in assessing P-glycoprotein functionality in the LLC-PK1, LLC-PK1:MDR1 and Caco-2 cell lines. Eur. J. Pharm. Sci. (2000) 11 207-214.
39. Lecureur V., Guillouzo A., Fardel O. Differential expression of the polyspecific drug transporter OCT1 in rat hepatocarcinoma cells. Cancer Lett. (1998) 126 227-233.
40. Wang D.S., Jonker J.W., Kato Y., Kusuhara H., Schinkel A.H., Sugiyama Y. Involvement of organic cation transporter 1 in hepatic and intestinal distribution of metformin. J. Pharmacol. Exp. Ther. (2002) 302 510-515.
41. Troutman M.D., Thakker D.R. Rhodamine 123 requires carrier-mediated influx for its activity as a P-glycoprotein substrate in Caco-2 cells. Pharm. Res. (2003) 20 1192-1199.
42. Cho C.W., Liu Y., Yan X., Henthorn T., Ng K.Y. Carrier-mediated uptake of rhodamine 123: implications on its use for MDR research. Biochem. Biophys. Res. Commun. (2000) 279 124-130.
43. Sonneveld P., Wiemer E. Assays for the analysis of P-glycoprotein in acute myeloid leukemia and CD34 subsets of AML blasts. Leukemia (1997) 11 1160-1165.
44. Hohage H., Stachon A., Feidt C., Hirsch J.R., Schlatter E. Regulation of organic cation transport in IHKE-1 and LLC-PK1 cells. Fluorometric studies with 4-(4-dimethylaminostyryl)-N-methylpyridinium. J. Pharmacol. Exp. Ther. (1998) 286 305-310.
45. Yasujima T., Ohta K., Inoue K., Yuasa H. Characterization of human OCT1-mediated transport of DAPI as a fluorescent probe substrate. J. Pharm. Sci. (2011) 100 4006-4012.
46. Shu Y., Sheardown S.A., Brown C. et al. Effect of genetic variation in the organic cation transporter 1 (OCT1) on metformin action. J. Clin. Invest. (2007) 117 1422-1431.
47. Tzvetkov M.V., Vormfelde S.V., Balen D. et al. The effects of genetic polymorphisms in the organic cation transporters OCT1, OCT2, and OCT3 on the renal clearance of metformin. Clin. Pharmacol. Ther. (2009) 86 299-306.
48. More S.S., Li S., Yee S.W. et al. Organic cation transporters modulate the uptake and cytotoxicity of picoplatin, a third-generation platinum analogue. Mol. Cancer Ther. (2010) 9 1058-1069.
49. Eechoute K., Sparreboom A., Burger H. et al. Drug transporters and imatinib treatment: implications for clinical practice. Clin. Cancer Res. (2011) 17 406-415.
50. Gupta S., Wulf G., Henjakovic M., Koepsell H., Burckhardt G., Hagos Y. Human organic cation transporter 1 is expressed in lymphoma cells and increases susceptibility to irinotecan and paclitaxel. J. Pharmacol. Exp. Ther. (2012) 341 16-23.
51. Yonezawa A., Inui K. Importance of the multidrug and toxin extrusion MATE/SLC47A family to pharmacokinetics, pharmacodynamics/toxicodynamics and pharmacogenomics. Br. J. Pharmacol. (2011) 164 1817-1825.
52. Engel K., Wang J. Interaction of organic cations with a newly identified plasma membrane monoamine transporter. Mol. Pharmacol. (2005) 68 1397-1407.
53. Otsuka M., Matsumoto T., Morimoto R., Arioka S., Omote H., Moriyama Y. A human transporter protein that mediates the final excretion step for toxic organic cations. Proc. Natl. Acad. Sci. USA (2005) 102 17923-17928.
54. Annaert P.P., Turncliff R.Z., Booth C.L., Thakker D.R., Brouwer K.L. P-glycoprotein-mediated in vitro biliary excretion in sandwich-cultured rat hepatocytes. Drug Metab. Dispos. (2001) 29 1277-1283.
55. Forster S., Thumser A.E., Hood S.R., Plant N. Characterization of rhodamine-123 as a tracer dye for use in in vitro drug transport assays. PLoS ONE (2012) 7 e33253.
56. Ciarimboli G., Struwe K., Arndt P. et al. Regulation of the human organic cation transporter hOCT1. J. Cell. Physiol. (2004) 201 420-428.
57. Ramadass R., Bereiter-Hahn J. How DASPMI reveals mitochondrial membrane potential: fluorescence decay kinetics and steady-state anisotropy in living cells. Biophys. J. (2008) 95 4068-4076.